JXB Advance Access originally published online on December 19, 2005
Journal of Experimental Botany 2006 57(2):303-317; doi:10.1093/jxb/erj040
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RESEARCH PAPER |
Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis?*
Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON M5S3B2 Canada
To whom correspondence should be addressed. E-mail: rsage{at}botany.utoronto.ca
Received 28 June 2005; Accepted 28 October 2005
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Abstract |
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 Top Abstract IntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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C4 photosynthesis is a complex specialization that enhances carbon gain in hot, often arid habitats where photorespiration rates can be high. Certain features unique to C4 photosynthesis may reduce the potential for phenotypic plasticity and photosynthetic acclimation to environmental change relative to what is possible with C3 photosynthesis. During acclimation, the structural and physiological integrity of the mesophyll–bundle sheath (M-BS) complex has to be maintained if C4 photosynthesis is to function efficiently in the new environment. Disruption of the M-BS structure could interfere with metabolic co-ordination between the C3 and C4 cycles, decrease metabolite flow rate between the tissues, increase CO2 leakage from the bundle sheath, and slow enzyme activity. C4 plants have substantial acclimation potential, but in most cases lag behind the acclimation responses in C3 plants. For example, some C4 species are unable to maintain high quantum yields when grown in low-light conditions. Others fail to reduce carboxylase content in shade, leaving substantial over-capacity of Rubisco and PEP carboxylase in place. Shade-tolerant C4 grasses lack the capacity for maintaining a high state of photosynthetic induction following sunflecks, and thus may be poorly suited to exploit subsequent sunflecks compared with C3 species. In total, the evidence indicates that C4 photosynthesis is less phenotypically plastic than C3 photosynthesis, and this may contribute to the more restricted ecological and geographical distribution of C4 plants across the Earth.
Key words: Acclimation, C3, C4 photosynthesis, phenotypic plasticity, sun–shade, temperature
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Introduction |
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TopAbstractIntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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Phenotypic plasticity refers to the ability of individual organisms to respond to environmental variation by altering their characteristics to compensate for, or acclimate to, variable environmental conditions (Pigliucci, 2001
). Organisms considered to be generalists have highly plastic phenotypes and are suited for a wide variety of conditions. They are thus more likely to acclimate and survive in unpredictable environments than less phenotypically plastic species. Organisms with low phenotypic plasticity are less likely to acclimate fully to environmental change, and thus tend to occur in less variable conditions than highly plastic organisms. In part because of a more uniform selection pressure, these organisms are often highly specialized for a restricted set of conditions, and are more fit than generalists within that environment. Increased specialization, however, may result in a loss of plasticity or acclimation potential. As a result, the more evolutionarily derived and specialized species could be more restricted in ecological and geographical distribution.
Within angiosperms, the CO2-concentrating mechanism of C4 photosynthesis represents a specialized adaptation derived from C3 ancestors. C4 photosynthesis has independently arisen over 45 times in a wide range of advanced angiosperm taxa (Sage, 2004). In almost all known C4 species, C4 photosynthesis requires the development of Kranz anatomy (Figs 1, 2; Dengler and Nelson, 1999). Despite the polyphyletic nature of C4 photosynthesis, certain anatomical features are common to most C4 plants, including: (i) specialization of two distinct photosynthetic tissue types: bundle sheath (BS) and mesophyll (M) tissue; (ii) the arrangement of BS cells near vascular tissue, with M peripheral to BS cells and adjacent to intercellular spaces; (iii) high vein density and a low ratio of M to BS (often 1:1), resulting in short diffusion pathways for C4 metabolites; and (iv) minimal CO2 leakage from BS cells, reflecting extensive contact between M and BS cells. Within C3 plants, the photosynthetic assimilation and reduction processes occur in both M and BS tissues, typically within a single photosynthetic cell; however, in C4 plants, M tissue assimilates CO2 to form organic acids that diffuse to the BS tissue (Fig. 1). In all cases, the evolution of the C4 pathway involved the modification of pre-existing biochemistry in C3 ancestors to enable the concentration of CO2 into the BS tissue compartment where the CO2-fixing enzyme Rubisco is localized (Hatch, 1987; Kanai and Edwards, 1999; Sage, 2004).
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Together, the modifications of metabolism and anatomy that allow for CO2 concentration represent a co-ordinated, specialized adaptation that enhances performance of C4 plants during periods of low atmospheric CO2 availability and in warm, often dry environments (Ehleringer et al., 1991
, 1997). As a derived specialization, however, the metabolic and structural requirements of the C4 pathway may have decreased the ability of C4 plants to modify the photosynthetic apparatus in order to acclimate and improve performance in altered environments. This paper explores the possibility that one cost of evolving C4 photosynthesis is a reduced potential for phenotypic plasticity and acclimation. |
Why should C4 plants have less acclimation potential than C3 plants? |
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TopAbstractIntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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The success of most plant species requires some ability to acclimate to environmental change, as environmental variation is inevitable (Schlichting, 1986
). In addressing acclimation potential between generalists and specialists, or in this paper, C3 versus C4 plants, the issue is one of relative degrees of acclimation, and whether barriers exist that might prevent highly plastic acclimation responses in C4 taxa. Specialist species may have inherent barriers that constrain or even prevent high phenotypic plasticity. The nature of these constraints is not well defined. Examination of C3 and C4 acclimation potentials may serve as a useful case study in how specialized adaptations affect phenotypic plasticity.
Conceptually, there are a number of reasons why C4 plants might not have the same ability to acclimate to low light, temperature variation, or elevated CO2 as C3 species. The C4 pathway requires close integration of distinct photosynthetic processes: PEP carboxylation and regeneration in M tissue with the Calvin cycle in BS tissue (Fig. 1). Failure to co-ordinate M and BS structure and function would reduce photosynthetic capacity and resource use efficiency (Leegood and Walker, 1999). At the structural level, disruption of M to BS tissue arrangements could increase diffusion distances, interfere with diffusion pathways, or enhance pathways for CO2 leakage from the BS cells. At the metabolic level, ineffective acclimation could lead to a loss of co-ordination between the C3 and C4 biochemical cycles. For example, if the C4 cycle reactions proceed faster than the C3 cycle following acclimation, too much CO2 would be pumped into the BS, building up the CO2 concentration to a point where leakage of CO2 out of the BS becomes substantial (von Caemmerer and Furbank, 1999). In effect, the C4 pump would begin to resemble a futile cycle and lose photosynthetic efficiency. Alternatively, if C4 cycle activity following acclimation is slow relative to the capacity of Rubisco and the C3 cycle, then BS CO2 levels would decline and photorespiration rates increase. To avoid these problems, acclimation of C4 photosynthesis has to involve co-ordinated changes between the M and BS tissues in order to maintain functional stoichiometries. By contrast, in C3 species, all photosynthetic cells are functionally equivalent, thereby allowing each cell to acclimate to a new environment in a more autonomous manner than should be possible in a C4 leaf. The simplicity of the C3 system relative to the C4 system, therefore, allows photosynthetic plasticity to be concentrated at the cellular rather than tissue levels, potentially allowing for greater acclimation ability in C3 leaves.
Photosynthetic acclimation brings the costs of tissue construction and maintenance in line with the probable photosynthetic carbon gain that a new environment can support (Mooney and Gulmon, 1982; Bloom et al., 1985; Sims et al., 1998a; Poorter et al., 2006). Because the photosynthetic unit in C3 plants is localized within autonomous cells, individual cells can be enlarged or reduced in size and number (in newly developing leaves) without compromising metabolic integrity. In C4 plants, the requirements to maintain functional relationships between the C3 and C4 cycles could constrain the extent to which tissue construction and maintenance costs are altered following environmental change. In addition, chloroplasts and other organelles in C4 leaves are spatially localized to either the interior third, or the outer periphery, of BS cells depending on photosynthetic biochemical subtype (Fig. 2; Dengler and Nelson, 1999). Organelle localization in the BS is essential because the ability to trap and refix CO2 before it can escape is enhanced by locating organelles near the vascular tissue (Kanai and Edwards, 1999). Localizing BS chloroplasts in such a manner restricts the total cell volume available to house Rubisco and the enzymes of the carbon reduction cycle. Changing the amount of these enzymes is an important part of the acclimation process in C3 plants (Anderson et al., 1988; Evans and Seemann, 1989; Leegood and Edwards, 1996), but may be constrained in C4 species by restrictions in organelle size and number. Modifications to organelle sizes and numbers in C4 plants may be difficult as it could interfere with ultrastructural arrangements required for an effective C4 pathway. In C3 plants, by contrast, all chlorenchyma cells are functionally equivalent in that all contain Rubisco and carbon reduction cycle enzymes. The C3 leaf is not restricted to packaging Rubisco into the relatively small space located at one end of the BS cells. If Rubisco activity becomes limiting in a C3 leaf, for example, the plant can compensate by increasing Rubisco content per chloroplast, creating more chloroplasts, or producing more cells in new leaves (Oguchi et al., 2005).
Acclimation requires the ability to sense environmental change and transduce it into an effective response. Photosynthetic acclimation is controlled by three general mechanisms: (i) environmental perception by sensory proteins such as phytochrome that activate a signal-transduction pathway, (ii) chloroplast-specific control that is linked to redox state, and (iii) carbohydrate, nutrient, and phytohormone signals that co-ordinate leaf and whole plant responses (Stitt and Krapp, 1999; Malakhov and Bowler, 2001; Lin and Shalitin, 2003; Long et al., 2004; Walters, 2005). In C3 plants, much of the control over the acclimation response is internal to the cell because redox state changes originate within chloroplasts and mitochondria (Anderson et al., 1995; Walters, 2005). Reliance on local command and control is problematic in C4 plants because of the need to co-ordinate M and BS responses; hence, an additional layer of regulatory control is probably required for an effective acclimation response. Furthermore, different promoter systems are required for the development of C4 tissue specialization (Dengler and Taylor, 2000; Matsuoka et al., 2001); therefore, acclimation responses may have to be transduced through additional promoter networks during development.
Alternatively, there may be no barriers associated with the photosynthetic pathway that inherently restrict phenotypic plasticity in C4 plants relative to C3 plants. Instead, low phenotypic plasticity may simply result from specialization for hot, high-light environments in the same manner that many C3 species specialized for these environments have low phenotypic plasticity. Because the main advantage of the C4 pathway occurs in conditions promoting photorespiration, it is probable that many C4 species are specialized for hot, high-light conditions and thus they may not be appropriate for assessing hypotheses regarding varying potential for phenotypic plasticity. There are situations, however, where a high degree of phenotypic plasticity would be advantageous to C4 plants. Numerous C4 species develop dense canopies where self-shading of older leaves is extensive. Acclimation to low light within a canopy is thus required if interior leaves are to maintain high resource-use efficiency and significantly contribute to carbon gain. In addition, a number of C4 species are successful in environments that are atypical for C4 photosynthesis, namely low-light and cooler habitats (Long, 1999; Sage et al., 1999). Although some adaptive specializations may have occurred in C4 species from cooler or low-light habitats, they may also show substantial phenotypic plasticity as most of these species occur in variable environments such as canopy gaps and high elevation (Brown, 1977; Smith and Martin, 1987b; Sage and Sage, 2002). A greater potential for phenotypic plasticity would probably be found in C4 plants from these variable environments.
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Acclimation of C3 and C4 photosynthesis to shade |
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TopAbstractIntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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Shade acclimation is the best-studied acclimation response of C3 photosynthesis, such that it now serves as a model of phenotypic plasticity in classrooms and textbooks. Shade-acclimation demonstrates the range of acclimation responses present in leaves (Table 1; Lambers et al., 1998
; Walters, 2005). At one level are the economic-type responses, where the activities of non-limiting processes are modulated to match activities of limiting processes (Bloom et al., 1985). Examples of economic-type responses are where the levels of Rubisco, carbon-reduction-cycle protein, enzymes for sucrose and starch synthesis, and electron-transport machinery are reduced following shading to match light-harvesting capacity (Table 1; Anderson et al., 1988; Evans, 1988; Bailey et al., 2004). At the leaf level, cell size, cell number, and leaf thickness are altered in newly formed leaves to bring construction and maintenance costs in line with the ability of the light environment to support the energetic costs (Björkman, 1981; Mooney and Gulmon, 1982; Evans and Seemann, 1989). Following shading, pigment levels shift as the levels of photo-protective carotenoids decline, while chlorophyll content increases (Bailey et al., 2004; Horton and Ruban, 2005). Acclimation also involves qualitative adjustments, such as the stacking of thylakoid membranes to enhance light capture and to create additional volume for proton storage (Sharkey et al., 1986). Some acclimation responses are rapid and reversible, such as chloroplast movements, while others are slow and largely irreversible, such as anatomical patterns established when leaves mature in a particular environment. With respect to C3 and C4 acclimation, the structural and economic-type responses are the most relevant for evaluating the potential for phenotypic plasticity. Acclimation responses involving changes in anatomy or enzyme complement are more likely to be linked to the photosynthetic pathway because C3 and C4 species inherently differ in these attributes.
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Using the well-described responses of C3 plants to shade as a reference (Table 1), it can be evaluated whether C4 plants have the same potential for shade acclimation as C3 photosynthesis. Two parameters of particular value in evaluating structural and biochemical acclimation are leaf thickness and Rubisco activity, respectively. A common acclimation response to shading is the thinning of leaves; hence, the relative degree of leaf thinning can be compared to examine whether there are inherent differences between the photosynthetic pathways that might be associated with anatomical requirements to maintain the M-BS stoichiometry. Second, Rubisco contents decline markedly during shade acclimation in C3 plants, on the basis of leaf area, chlorophyll, and leaf nitrogen content (Evans, 1988
; Evans and Seemann, 1989). Because Rubisco activity is non-limiting in shaded C4 leaves, significant reductions in Rubisco content should also occur during shade acclimation if resource use efficiency is to be maintained (von Caemmerer and Furbank, 1999).
No consistent differences are apparent in the ability of C3 and C4 species to reduce leaf thickness following shading. Comparisons of leaves produced at high light and low light generally show that leaf thickness declines by 30–50% in both C3 and C4 species (Louwerse and Zweerde, 1977; Ward and Woolhouse, 1986a). In a direct comparison of Phaseolus vulgaris (C3) and Zea mays (C4), the reduction in leaf thickness from high light to low light was 34% for the C3 plants and 32% in maize (Louwerse and Vanderzweerde, 1977). Exceptions have been noted, for example, in Amaranthus retroflexus, a sun-adapted C4 plant with extensive self-shading, there is little difference in the thickness of leaves from high- and low-light-grown plants (Tazoe et al., 2005).
Rubisco content in C4 plants does not appear to be as responsive to changes in light availability as in C3 plants, particularly in terms of the percentage of leaf nitrogen invested in Rubisco. In numerous C3 species, Rubisco content or activity is reduced by over 55% in shaded compared to high-light grown leaves (Table 2). By contrast, the degree of reduction is generally less in C4 species, being 10–54% when Rubisco content or activity is expressed on a chlorophyll basis (Table 2). In terms of the percentage of nitrogen allocated to Rubisco, there is modest (about 15%) reduction in Rubisco content per unit nitrogen in Amaranthus retroflexus between high- and low-light-grown plants (Tazoe et al., 2005). The fraction of nitrogen in Rubisco increases in maize and Paspalum leaves grown in low light (50 µmol photons m–2 s–1) compared with high-light (1000 µmol photons m–2 s–1; this observation is based on Rubisco: protein ratios derived from Ward and Woolhouse, 1986b). These results indicate that C4 plants have a low ability to reduce their allocation of nitrogen to Rubisco following shading, in contrast to the typical C3 response where the allocation of leaf nitrogen to Rubisco declines substantially (>50%) in low compared to high-light-grown leaves (Seemann et al., 1987; Evans and Seemann, 1989).
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An expensive component of a leaf is the vascular tissue, both from the greater investment costs (lignin is one of the most energetically-expensive molecules in plants), and because non-photosynthetic vascular tissue replaces photosynthetic cells, thereby reducing the light-absorbing capacity of the leaf. In low light, the rate of transpiration is reduced, and with it, the need for an extensive vascular network. Consequently, vein density can decline in shaded C3 plants, allowing M cells to occupy a greater proportion of the leaf area (Wylie, 1939
, 1951; Bjorkman et al., 1972; Boardman, 1977; Jurick et al., 1982). By contrast, C4 plants must maintain a high vein density and tight vein spacing because of the requirement for close proximity of M and vein-associated BS cells. C4 grasses have, on average, interveinal distance (IVD) values that are less than half that of C3 grasses (Crookston and Moss, 1974; Morgan and Brown, 1979; Hattersley and Watson, 1975; Kawamitsu et al., 1985; Dengler et al., 1994). The average C4 grass IVD is 120 µm, whereas the average IVD of C3 grasses is 280 µm (values estimated from Dengler et al., 1994; Ogle, 2003). Veins in C4 grasses are spaced 50–200 µm apart, while in C3 plants they are 200–400 µm apart (Ogle, 2003). The lower IVD values in C4 grasses are correlated with decreases in M:BS tissue volume ratios compared with C3 grasses (Hattersley, 1984; Dengler et al., 1994). This has also been formalized for C4 grasses where M cells are no more than ‘one cell distant’ from BS cells (Hattersley and Watson, 1975). Similar patterns in C4 dicot species compared with C3 dicot species have also been reported (Rao and Rajendrudu, 1989).
In low-light environments, there is an energetic cost associated with widely-spaced veins in C4 plants, as indicated by surveys showing the quantum yield is lower in species with greater IVD (Fig. 3; Ogle, 2003). By contrast, quantum yield is independent of vein spacing in C3 plants (Fig. 3). Carbon-isotope discrimination increases in shaded C4 plants with wider vein spacing, indicating greater leakage of CO2 out of the bundle sheath (Ogle, 2003). The increase in CO2 leakage is probably responsible for the decline in the quantum yield of the C4 species with greater vein spacing (Ogle, 2003). Reducing vein density as a means of shade-acclimation is not a restriction for C3 leaves, but could be for C4 leaves as it can compromise the efficiency of the C4 apparatus.
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Direct tests of growth light intensity on vein spacing of closely-related C3 and C4 species are not apparent in the literature, so a study was established to examine shade responses of leaf anatomy and vein pattern in C3 and C4 species of the dicot genus Flaveria. Flaveria species are valuable for comparing the effect of C4 evolution on various characteristics in plants, because the C3 species is ancestral to the derived C4 species (McKown et al., 2005
) and the weedy C3 and C4 species in this genus occur in roughly similar habitats (Powell, 1978). Leaf thickness, vein density, IVD, M tissue area, BS tissue area, and M:BS ratios were compared between F. australasica (C4) and F. robusta (C3) plants grown in a growth chamber at either 500 µmol photons m–2 s–1 or 100 µmol photons m–2 s–1. Far red-to-red ratios were also lowered to mimic natural shading using plastic filters, thereby inducing the full range of shade acclimation responses seen in natural situations (Lee, 1985). Leaf thickness declined proportionally more in the C3 than in the C4 species (Figs 4, 5a). In C3 F. robusta, vein density and IVD changed little while significant changes occurred in the C4 F. australasica (Fig. 5b, c). In the C4 species, the reduction in vein density was approximately 20%. Mesophyll and BS tissue areas in leaf cross-sections decreased in both species, but the change in cross-sectional area (which indicates changes in tissue volume) was greater in the C3 F. robusta (Fig. 5d, e). Intercellular spaces (ICS) increased and BS exposure to ICS doubled from 4.6% to 10.5% (P <0.0001) in the shaded C4 F. australasica plants (data not shown), indicating there is a greater potential for CO2 leakage out of the BS directly into the intercellular air spaces. This hypothesis is supported by carbon isotope measurements. Flaveria australasica plants grown in the shade had a lower carbon isotope ratio (–16.0 per mil) than plants grown in bright light (–15.2 per mil; P <0.05: the plant were grown as described in the legend of Fig. 5). The more negative isotopic values for the shade-grown C4 leaves indicate a greater degree of CO2 leakage from the bundle sheath (von Cammerer et al., 1997). Similarly, Amaranthus retroflexus grown in shade and at high nitrogen also shows a reduction in vein density that is correlated with a decrease in the carbon-isotope ratio (Tazoe et al., 2005). When the mean IVD values from the C4 Flaveria species are plotted on the quantum yield versus IVD relationship developed for grasses (Fig. 3), then the predicted reduction in quantum yield is modest (about 9%); however, the importance of this decline is substantial, since the quantum yield advantages of C4 over C3 dicot species at 30 °C (0.061 mol CO2 mol–1 photons for C4 versus 0.052 mol mol–1 for C3 dicots; Ehleringer and Pearcy, 1983) would be halved. Quantum yield differences between C3 and C4 species are important for understanding the relative performance of C3 versus C4 photosynthesis in low-light and variable thermal environments (Ehleringer and Pearcy, 1983; Ehleringer et al., 1997).
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Flaveria, Zea mays, and Amaranthus are sun-adapted plants; they may acclimate to low light (as during self-shading), but would not be able to complete their life cycle in the shade of a forest canopy (Björkman, 1981
). Sun-adapted plants are generally considered specialists for open environments and, as such, comparisons involving only sun-plants may not show the full range of acclimation that could be seen in a true generalist species. Hence, generalist species should also be considered if the potential of C4 plants to acclimate to low light is to be fully evaluated. Many C4 species persist in heavily shaded environments (Brown, 1977; Pearcy and Calkin, 1983; Long, 1999) indicating they either possess a substantial capacity for shade acclimation, or they are truly shade-adapted (Horton and Neufeld, 1998; Sage and Pearcy, 2000). Based on floristic descriptions, it does not appear that the majority of these species are shade specialists, as they also occur along canopy openings such as paths or tree-fall gaps, and most can also occur in partially open habitats. For example, in the Flora of the Guianas (Judziewicz, 1990; the Guianas occur in the wet-tropics of northern South America), no C4 grass species is described as being localized in forest interiors, while 34% of the C3 grass flora is described as such (Sage, 2000). One per cent of the C4 grass flora of the Guianas is described as occurring along forest margins. These particular species represent the sun–shade generalists, and would be the best group to examine shade acclimation potentials in the C4 flora.
In contrast to sun-adapted C4 species (such as Flaveria), shade-tolerant C4 grasses are able to maintain close vein spacing under shaded conditions, for example, in Microstegium vimineum (Winter et al., 1982), Muhlenbergia frondosa, M. sobolifera, M. schreberi (Smith and Martin, 1987a), Paspalum conjugatum (Ward and Woolhouse, 1986a, b), and Rottboellia exaltata (Paul and Patterson, 1980). Instead of increasing, IVD decreases in Muhlenbergia frondosa and Rottboellia exaltata as M and BS cells do not expand to normal size. Reductions in the size of BS and M cells have also been observed in Paspalum conjugatum relative to Zea mays grown in shade (Ward and Woolhouse, 1986a, b). Ogle (2003) suggested that surviving shade conditions with sufficient quantum yield involves maintaining a threshold IVD lower than that observed in most C4 species. The shade-adapted species of Microstegium, Muhlenbergia, and Paspalum have much lower IVD values than the average reported for C4 grasses, respectively, 72 µm (Winter et al., 1982), 73 µm (Smith and Martin, 1987a), and 78 µm (Kawamitsu et al., 1985).
A particularly interesting case of maintaining low IVD is observed in the shade-tolerant dicot, Chamaesyce herbstii (formerly Euphorbia forbesii) from the Hawaiian Islands (Herbst, 1972; Pearcy, 1983). Chamaesyce herbstii is a small-to-medium stature tree that is scattered in the understory of mesic Hawaiian forests (Koutnik and Huft, 1990). During normal leaf development in shaded C. herbstii, a number of ‘disjunct’ veins arise, consisting of isolated xylem tracheids (Herbst, 1972). There is no physical connection between the vein ‘islands’ and the rest of the leaf venation, yet normal BS develops around these disjunct veins. C4 dicots are generally not shade-tolerant, so this unique solution to the problem of maintaining close vein spacing and M:BS ratios exemplifies the challenge posed by the C4 pathway during low-light acclimation. In a direct comparison of physiological acclimation to shade in C. herbstii with the co-occurring understory C3 tree, Claoxylon sandwicense, grown under identical high- and low-light conditions, Pearcy and Franceschi (1986) observed that the shade-grown C3 species reduced the dark respiration and electron-transport rates to a greater relative degree than shade-grown Chamaesyce herbstii (Table 3). Leaf chlorophyll content declined little in Chamaesyce herbstii, while it rose in Claoxylon sandwicense. Increased chlorophyll content is indicative of a greater ability to harvest photons in low light (Evans, 1988; Evans and Seemann, 1989). The result of these changes is that the C3 species in low-light environments has a lower light-compensation point than the C4 species, indicating a greater tolerance for shaded conditions (Table 3).
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The shade-tolerant C4 grass Microstegium vimineum is a summer-active species that occurs in gaps and understoreys in deciduous forests (Horton and Neufeld, 1998
). In the eastern US, M. vimineum is a serious invasive species that can displace native C3 herbs in shaded habitats within the forest. Shade-acclimation of M. vimineum has not been directly compared with that of C3 species, but a number of patterns stand out that indicate it has less potential to acclimate to low-light environments than similar C3 species. Winter et al. (1982) observed typical patterns of shade acclimation in terms of leaf thickness and leaf area responses, but not carboxylating enzymes (Table 4). Rubisco activity rose slightly from high to low light, while PEPCase activity was unchanged. The failure of carboxylating enzymes to adjust to low-light conditions is a sign of limited acclimation potential in this shade-tolerant grass.
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Horton and Neufeld (1998)
characterized the ability of Microstegium vimineum to utilize sunflecks (short episodes of high light that shine through small canopy gaps). Most sunflecks last between a few seconds to a few minutes, and often represent the major source of photons in the understorey. The ability to capture and store light energy in a sunfleck is an important component of shade-tolerance (Sharkey et al., 1986; Pearcy et al., 1996, 1997). Utilization of sunflecks is related to the ability of a leaf to keep its photosynthetic apparatus in an active, induced state, ready to use the photonic energy in a sunfleck. Normally, photosynthetic enzymes deactivate following shading and, once deactivated, several minutes are required for reactivation (Sharkey et al., 1986; Sage et al., 1993; Pearcy et al., 1996). In the deactivated state, the photosynthetic apparatus cannot use most of the photons in a light fleck. If induction requires more than a minute or so, most sunflecks would not be exploited. Shade-adapted C3 plants are able to maintain the leaf in a partially induced state for the better part of an hour after the last sunfleck has passed. In Alocasia macrorrhiza, an understorey C3 species from northern Australia, the half-time for relaxation of the induction state of photosynthesis is 30 min (Chazdon and Pearcy, 1986). By contrast, it is just 2.4 min in the C4 Microstegium vimineum (Horton and Neufeld, 1998). This result indicates that shade-tolerant C4 plants do not maintain the ability to exploit sunflecks for more than a few minutes after the last sunfleck has passed, while in understorey C3 species, the photosynthetic apparatus remains primed and ready for action for a considerably longer period. Failure of C4 plants to maintain leaves in an induced state as well as shade-adapted C3 plants could be associated with the additional requirement to maintain high activation of the C4 cycle in addition to the C3 cycle. High activation of the C4 cycle would entail maintaining high gradients between the metabolite pools of the M and BS compartments, as well as maintaining activated forms of PEP carboxylase, pyruvate-phosphate dikinase and other C4 cycle enzymes.
The sun-plant Zea mays also uses sunflecks less efficiently than C3 plants such as soybean and Alocasia, particularly short duration sunflecks (<10 s; Krall and Pearcy, 1993). In C3 plants, the photosynthesis rate increases as lightfleck duration falls below 10 s, while in maize it decreases. Much of the stored energy in short-duration lightflecks is apparently not used in C4 plants due to a breakdown in the co-ordinated metabolism of the C3 and C4 cycles. Krall and Pearcy (1993) propose that the decline in maize photosynthesis during short duration sunflecks results from a burst of CO2 leaving the BS cells. This is caused by the C4-cycle reactions moving CO2 into the BS faster than the deactivated C3-cycle reactions can utilize it. The inability to maintain a high activation state of the C3 cycle in maize appears to create conditions favouring the futile cycling of CO2 during short-duration sunflecks (Krall and Pearcy, 1993).
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Temperature acclimation |
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TopAbstractIntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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Research on temperature acclimation has emphasized responses to thermal extremes. Responses to thermal extremes do not obviously vary between photosynthetic pathways, so there is little reason to expect acclimation to extreme temperatures to be inherently different between ecologically similar C3 and C4 plants. There have been hypotheses that C4 species are more prone to chilling injury because C4-cycle enzymes can be cold-labile (Long, 1983
; Potvin et al., 1986). Recent studies show that the C4-cycle enzymes from cold-tolerant C4 plants are stable in chilling conditions (Simon and Hatch, 1994; Matsuba et al., 1997; Long, 1999; Pittermann and Sage, 2000), demonstrating that chilling sensitivity is not an inherent feature of the C4 pathway. In contrast to responses to thermal extremes, there may be inherent differences in the acclimation response of C3 and C4 photosynthesis to non-stressful temperature variation. C4 plants exhibit a different pattern of biochemical limitation across a range of temperatures than C3 species (von Caemmerer, 2000; Sage, 2002; Kubien et al., 2003) which should alter the nature of the acclimation response between the two pathways.
Thermal acclimation to low temperature in C3 plants often involves an enhancement of the photosynthetic rate below the thermal optimum (Slatyer, 1977; Berry and Raison, 1981; Mawson and Cummings, 1989; Savitch et al., 1997; Strand et al., 1999; Yamasaki et al., 2002; Yamori et al., 2005). In C4 plants, early acclimation studies observed an enhancement in photosynthesis at cooler temperatures in desert species grown in moderate conditions (Pearcy, 1977; Berry and Raison, 1981). However, these studies often compared plants grown near 20 °C with species grown under hot (>40 °C) conditions, so that the thermal acclimation observed may have been more a case of heat acclimation than low-temperature acclimation. Recent studies of C4 performance below 20 °C indicate little change in the photosynthetic rate of cold-tolerant C4 plants upon growth in cool conditions (Matsuba et al., 1997; Pittermann and Sage, 2001; Cavaco et al., 2003; Naidu et al., 2003; Naidu and Long, 2004; Kubien and Sage, 2004a).
C4 photosynthesis is well recognized to be inhibited by low temperatures to a greater degree than C3 photosynthesis (Berry and Raison, 1981). Three leading hypotheses have been proposed to explain poor photosynthetic performance at low temperature in C4 leaves. First, the activity of the C4-cycle enzymes PEPCase and PPDK decline due to a cold-induced lability of these enzymes (Long, 1983, 1999). This hypothesis may explain poor photosynthetic performance in species from warm regions, but C4 species that are naturally cold-tolerant do not show declines in PPDK or PEPCase activity with prolonged cold exposure (Simon and Hatch, 1994; Usami et al., 1995; Matsuba et al., 1997; Pitterman and Sage, 2000). Hence, this limitation is not the obvious problem that necessarily prevents the C4 pathway from performing in cool climates. Second, the maximum quantum yield of C4 photosynthesis is less than that of C3 species in cooler environments, due to the additional energy cost of running the C4 pump (Ehleringer and Pearcy, 1983). This is proposed to be an inherent limitation on C4 plants in the cold (Ehleringer et al., 1997), but this constraint would mainly be an issue in low-light environments. At high light, where most C4 species are found (including most of the cold-tolerant C4 species), the quantum yield differences are not directly relevant, because there is an excess of photons, and much of the absorbed light energy is given off as heat (Kubien and Sage, 2004b). Therefore, quantum yield differences can contribute, but are not the main cause of poor C4 photosynthetic performance in low temperature conditions (Sage and Kubien, 2003).
In cold-tolerant C4 species, Rubisco capacity becomes limiting at low temperature and imposes a ceiling on photosynthetic rate below 20 °C (Pearcy, 1977; Pittermann and Sage, 2000; Sage, 2002; Kubien et al., 2003). Rubisco capacity in vitro and gross photosynthesis become the same in a variety of C4 species below 20 °C which should be the case if Rubisco controls the rate of CO2 assimilation in C4 plants (Fig. 6). Fluorescence and gas exchange measurements show that the ratio of 
PSII/CO2 increases at low temperature where Rubisco capacity and the gross photosynthesis rate are equivalent (Fig. 7; Kubien et al., 2003, Kubien and Sage, 2004a). PSII/CO2 should rise with increasing leakiness of CO2, because leakage of CO2 does not affect the photochemical yield of PSII, but does reduce the quantum yield of CO2 fixation (von Caemmerer et al., 1997). Increased CO2 leakage from the C4 BS cells is consistent with Rubisco dominating the control of photosynthesis at low temperature. When Rubisco capacity is limiting, the C4 cycle pumps CO2 into the BS faster than it can be fixed by Rubisco, causing the BS CO2 concentration and the leak rate to increase (Kubien et al., 2003).
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If Rubisco is the leading limitation on C4 photosynthesis at low temperature, then the main way to improve photosynthesis would be to increase Rubisco content by packing more Rubisco into the fraction of the BS where chloroplasts are localized. There is little evidence that this occurs. In most C4 species examined, cold-acclimation is not accompanied by increased or varied Rubisco capacity. In the montane grass Muhlenbergia montanum, which grows above 3000 m in the Rocky Mountains of the USA, and the boreal-zone C4 grass Muhlenbergia glomerata, Rubisco content is unchanged in warm- and cold-grown plants (Fig. 6; Pittermann and Sage, 2001
; Kubien and Sage, 2004a). Shortly after transferring M. montanum to low temperature, there is a marked inhibition of photosynthesis, but only at warm measurement temperatures where Rubisco is not limiting (Pittermann and Sage, 2001). Within a few days of the transfer, the assimilation rate at elevated measurement temperatures has fully recovered to similar rates as before the transfer, indicating acclimation repairs inhibitions in PEP regeneration, PEP carboxylation, or electron transport that arise shortly after transfer to cool conditions (Pittermann and Sage, 2001). In Miscanthus giganteus, a montane C4 grass from eastern Asia that exhibits high productivity in cooler environments, Rubisco capacity changes little in plants grown at cool relative to warm temperature (Naidu and Long, 2004). Similar patterns have been observed in the cold-tolerant C4 grasses Spartina anglica and Paspalum dilatatum (Matsuba et al., 1997; Cavaco et al., 2003). By contrast, in the chilling-sensitive species Zea mays and Zoysia japonica, Rubisco contents decline substantially with prolonged exposure to chilling conditions, along with the photochemical capacity and the activity of C4-cycle enzymes (Matsuba et al., 1997; Naidu et al., 2003; Naidu and Long, 2004).
In summary, there is little evidence that C4 species compensate for low-temperature exposure by building up Rubisco content to overcome a strong limitation caused by low Rubisco activity. Instead, cold-tolerant C4 plants are able to maintain Rubisco content and photosynthetic capacity, in contrast to cold-sensitive C4 species where numerous components of the photosynthetic apparatus degrade with prolonged exposure to cool conditions. Cold-tolerant C4 grasses have a pronounced ability to acclimate to chilling conditions qualitatively, as indicated by carotenoid changes that show they have well-developed mechanisms that protect against photoinhibition at low temperature (Kubien and Sage, 2004a).
In contrast to C4 species, C3 species show substantial acclimation to low temperature that involves increases in enzyme content. In C3 plants, the ability to regenerate Pi for photophosphorylation becomes a major limitation at low temperature (Sharkey, 1985; Sage and Sharkey, 1987; Falk et al., 1996; Strand et al., 1999). Acclimation to low temperature involves a partial, if not complete, removal of the Pi-regeneration limitation. This is brought about by increasing enzyme capacity for starch and sucrose synthesis relative to Rubisco capacity and the capacity for RuBP regeneration, or a change in the internal Pi status in leaves which improves Pi regeneration in low-temperature conditions (Leegood and Edwards, 1996; Stitt and Hurry, 2002; Hendrickson et al., 2004). Improving Pi-regeneration capacity often increases photosynthetic capacity at low temperature (Savitch et al., 1997; Strand et al., 1999). The limitation that dominates the rate of photosynthesis after acclimation increases the Pi-regeneration capacity is unclear. At lower CO2 levels than at present, Rubisco capacity can become limiting at cooler temperatures, and hence acclimation may involve an increase in Rubisco content (Sage, 2002). Consistently, Rubisco levels often increase at low temperature, and this is associated with increased rates of CO2 assimilation in cold-acclimated leaves (Strand et al., 1999; Yamori et al., 2005). Electron-transport capacity also increases at low temperature, such that limitations caused by a deficient electron transport capacity are alleviated (Mawson and Cummings, 1989; Savitch et al., 1997). This limitation could be particularly important in CO2-enriched atmospheres when the capacity for RuBP regeneration is the primary limitation.
Limitations controlling photosynthesis at elevated temperature remain unclear. Rubisco activase is reported to dissociate above the thermal optimum in both C3 and C4 species, creating a limitation on photosynthesis from a low activation state of Rubisco (Crafts-Brandner and Salvucci, 2002; Salvucci and Crafts-Brandner, 2004). Acclimation to elevated temperature in C3 plants involves stabilization of Rubisco activase, in part by the increased presence of a longer, more heat-stable isoform of activase (Law et al., 2001; Portis, 2003). Similar mechanisms appear to be present in maize, as acclimation to elevated temperature is associated with expression of a larger isoform of Rubisco and partial recovery of the Rubisco activation state (Crafts-Brandner and Salvucci, 2002). Electron-transport capacity can also become limiting for photosynthesis at elevated temperature in numerous C3 species adapted to warm climates (Bukhov et al., 1999; Schrader et al., 2004; Wise et al., 2004; Sharkey, 2005; Cen and Sage, 2005). The relative importance of limitations in electron transport capacity versus activation state remain uncertain. In C4 species, the uncertain nature of the limiting processes at elevated temperature is a large part of the overall problem in understanding acclimation of C4 plants to heat. In addition to the Rubisco activase and activation state limitations, photosynthesis may be limited by electron transport, PEP carboxylation, and PEP regeneration at elevated temperature (Sage, 2002; Kubien et al., 2003). Without a clear picture of the limitations on C4 photosynthesis at elevated temperature, it is difficult to assess how C4 leaves acclimate to heat in terms of the biochemical reactions that determine photosynthetic capacity.
In summary, the limited amount of work on low-temperature acclimation in C4 photosynthesis shows there is little enhancement of Rubisco capacity, as should be the case if a widespread limitation in Rubisco capacity is to be overcome. C3 species do show substantial acclimation, and this is often explained by increases in Pi regeneration capacity and Rubisco content. The difference in thermal acclimation between C3 and C4 species is consistent with the hypothesis that the relatively low volume of leaves devoted to Rubisco-containing chloroplasts restricts the ability of C4 species to compensate for low temperature by increasing Rubisco content. By contrast, C3 species lack this restriction, and appear to have a greater ability to pack in extra enzyme as needed. Thus, there is evidence indicating that C4 species may be constrained by their unique structural requirements to have a lower potential to acclimate to cooler temperatures than C3 leaves. This could have consequences for the overall performance of C4 species in environments where cool temperatures are common throughout the growing season.
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Acclimation to elevated atmospheric CO2 partial pressure |
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TopAbstractIntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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Acclimation of photosynthesis to atmospheric CO2 variation deserves brief mention, largely because C3 and C4 plants respond differently to increases in atmospheric CO2 content, although neither C3 nor C4 species show acclimation responses that are directly linked to CO2 level. Instead, the CO2 effect on the photosynthetic biochemistry is largely mediated by carbohydrate accumulation in leaves under conditions where carbon sinks in the plant are also experiencing high carbon supply (Sims et al., 1998b; Long et al., 2004
). C3 species show a greater degree of acclimation to elevated CO2 partial pressure than C4 species, largely because C3 photosynthesis is stimulated more by rising CO2, and hence the degree to which carbohydrate supply becomes excessive is potentially greater in the C3 species (Sage, 1994). In C3 species, there is a general decline in photosynthetic enzyme content with prolonged exposure to high CO2; Rubisco is preferentially reduced during early phases of acclimation, but most photosynthetic genes are switched off after long-term exposure, particularly when sink limitations are substantial (Sage and Coleman, 2001; Long et al., 2004). In C4 plants, acclimation is often negligible due to the lack of a strong response to increased CO2 partial pressure that is common in C4 plants (Sage and Kubien, 2003). C4 photosynthesis is CO2-saturated, or almost CO2-saturated at current atmospheric CO2 levels, so a strong response is not expected. This feature of the C4 photosynthetic pathway largely explains the relative lack of acclimation to rising CO2 level in C4 plants. However, certain C4 species show a slight to modest short-term stimulation of photosynthesis by increased CO2 availability, particularly under certain environmental conditions such as higher temperature and reduced mineral nutrition that increase the CO2 saturation point of photosynthesis (Ziska et al., 1999; Ghannoum et al., 2000; Sage and Kubien, 2003). Where CO2 stimulates photosynthesis, CO2 acclimation can be observed, typically as a slight reduction in photosynthesis at both high and low levels of CO2 (Tissue et al., 1995; LeCain and Morgan, 1998; Watling et al., 2000; Sage and Kubien, 2003). Acclimation may preferentially reduce the C4 cycle, as indicated by a reduction of PEPCase but not Rubisco content in Sorghum bicolor, Zea mays, and Flaveria species grown at elevated CO2 (Watling et al., 2000; Gascoigne-Owens et al., 2002; Snowdon et al., 2002). |
The consequence of reduced phenotypic plasticity in C4 plants |
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TopAbstractIntroductionWhy should C4 plants...Acclimation of C3 and...Temperature acclimationAcclimation to elevated...The consequence of reduced...References |
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Compared with C3 species, C4 plants have a restricted ecological and biogeographical distribution (Sage et al., 1999
). C4 species are absent from polar biomes, rare if not absent in cool temperate to boreal biomes, rare in alpine and montane elevations at all latitudes, and uncommon in forest understoreys. C4 photosynthesis is absent from certain plant life-forms, notably, canopy-forming forest trees. It is uncommon in short-stature trees, and in most shrub species, such that the woodland vegetation of the planet is almost exclusively C3 plants. The only regions where C4 photosynthesis is common in woody vegetation are in desert shrubs of saline soils and sand dunes. The reasons for the infrequency of C4 photosynthesis in these regions and life-forms has never been adequately explained, although it is recognized that there are a number of contributing factors (Sage and Pearcy, 2000). For example, in low-light environments, a higher energy requirement for C4 photosynthesis is an important consideration. This does not fully explain why there are so few shade-tolerant C4 species, because the quantum yield of C4 species is greater in warm environments (Ehleringer and Pearcy, 1983; Pearcy and Ehleringer, 1984). To the list of factors contributing to a lack of C4 plants in cool or shaded environments, it is proposed that a reduced potential for phenotypic plasticity should be added. In many ways, C4 plants show potential for acclimation, indicating that they are not too specialized for hot, high-light conditions to adjust to other environments. When the full suite of acclimation characteristics to low light or elevated temperature are considered, however, C4 plants appear to be deficient in one or more traits when compared with C3 species. For example, C4 plants do not seem to have the same capacity to modulate Rubisco content, nor do they appear to be able to keep the leaf biochemistry as induced following sunflecks as well as C3 plants. At the structural level, a requirement for high vein density may restrict acclimation potential to low light intensity. C4 species can modulate leaf thickness as well as C3 species, but appear to have extra costs when vein spacing is modified. Furthermore, a limited bundle-sheath volume may impose a space constraint on enzyme content, thus restricting the ability to increase Rubisco and other enzymes in situations where they may become limiting, such as low temperature. In summary, there is substantial evidence that C4 plants have inherent constraints that prevent them from acclimating to environmental change as well as C3 species, and this may have consequences for the range of life forms and landscapes where C4 photosynthesis can occur. |
Acknowledgements |
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We thank Professor Nancy Dengler for her valuable suggestions on this project. Publication of this work was supported by NSERC grant OGP0154273 to RFS and an NSERC post-graduate scholarship to ADM.
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Footnotes |
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* This paper is dedicated to Professor Nancy Dengler on the occasion of her retirement on 1 July, 2005.
Abbreviations: BS, bundle sheath; IVD, interveinal distance; M, mesophyll.
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